Various studies and researchers have
proposed a link between contagious yawning and
empathy, yet the conceptual basis for the
proposed connection is not clear and deserves
critical evaluation. Therefore, the authors
systematically examined the available empirical
evidence addressing this association; i.e., a
critical review of studies on inter-individual
differences in contagion and self-reported
values of empathy, differences in contagion
based on familiarity or sex, and differences in
contagion among individuals with psychological
disorders, as well as developmental research,
and brain imaging and neurophysiological
studies.

In doing so, they reveal a pattern of
inconsistent and inconclusive evidence regarding
the connection between contagious yawning and
empathy. Furthermore, they identify study
limitations and confounding variables, such as
visual attention and social inhibition. Future
research examining links between contagious
yawning and empathy requires more rigorous
investigation involving objective measurements
to explicitly test for this connection.

Yawning is characterized by a powerful
gaping of the jaw with deep inspiration,
followed by a temporary period of peak muscle
contraction with a passive closure of the jaw
during expiration (Barbizet, 1958). Yawns are
not under conscious control and, once initiated,
go to completion with minimal influence of
sensory feedback (Provine, 1986). Yawns have a
more complex spatio-temporal organization than
simple reflexes, and activate disparate
physiological systems. In humans, yawns produce
extended stretching of the orofacial
musculoskeleton; are accompanied by head
tilting, eye closure, tearing, salivating, and
opening of the Eustachian tubes in the middle
ear; and generate significant cardiovascular
changes (Provine, 2012).

Yawning appears to be a universal human act
that occurs throughout the lifespan, with an
average duration of between four and seven
seconds per yawn (Askenasy, 1989; Baenninger and
Greco, 1991; Barbizet, 1958; Gallup et al.,
2016a; Provine, 1986). Self-report studies
indicate that people yawn between six and 23
times per day, which depends upon an
individual's circadian rhythm or chronotype
(Baenninger et al., 1996; Provine et al., 1987a;
Zilli et al., 2007). Evolutionarily conserved,
yawning or a similar form of mandibular gaping
behavior has been observed in all classes of
vertebrates (Baenninger, 1987; Craemer, 1924;
Gallup et al., 2009; Luttenberger, 1975). As
further evidence that yawns are most probably
phylogenetically old, ontogenetically this
response occurs as early as 11 weeks gestation
in humans (de Vries et al., 1982).

While the neural structures necessary for
yawning appear to be located within the
brainstem (Heusner, 1946), a recent case study
demonstrated that electrical stimulation of the
putamen, which has extensive connectivity
between the brain stem and cortical regions,
induces yawning in humans (Joshi et al., 2017).
Pharmacological research on non-human animals
indicates yawning is under the control of
several neurotransmitters and neuropeptides in
the paraventricular nucleus (PVN) of the
hypothalamus; yawning is induced by dopamine,
nitric oxide, excitatory amino acids,
acetylcholine, serotonin, adrenocorticotropic
hormone-related peptides, and oxytocin, and is
inhibited by opioid peptides (Argiolas and
Melis, 1998; Daquin et al., 2001). A more recent
review has identified at least three distinct
neural pathways involved in the induction of
yawning, all of which converge on the
cholinergic neurons within the hippocampus
(Collins and Eguibar, 2010). Abnormal or
frequent yawning is symptomatic of numerous
pathologies, including migraine headaches,
stress and anxiety, head trauma and stroke,
basal ganglia disorders, focal brain lesions,
epilepsy, multiple sclerosis, schizophrenia,
sopite syndrome, and even gastro-intestinal and
some infectious diseases (reviewed by Daquin et
al., 2001; Gallup and Gallup, 2008; Walusinski,
2010). Yawning has also been thought to be an
indicator of hemorrhage (Nash, 1942), motion
sickness (Graybiel and Knepton, 1976),
encephalitis (Wilson, 1940), and rises in
cortisol (Thompson, 2011). The multifaceted
motor expression and activation of yawning
suggests it has a fundamental neurophysiological
significance. Consistent with this view, recent
comparative research demonstrates that across
mammals species' average yawn durations are
robustly correlated with their average brain
weight and cortical neuron number (Gallup et
al., 2016a).

Attempts to identify the physiological
function of yawning provide little consensus.
Yawning has been hard to characterize
functionally, primarily because there are
numerous eliciting stimuli. Smith (1999)
outlined over 20 functional hypotheses for why
we yawn; however, few have received empirical
support. Hypotheses range from increasing
alertness (Baenninger and Greco, 1991;
Baenninger et al., 1996), to inducing relaxation
of social tension in groups (Sauer and Sauer,
1967), and to aiding in the removal of
potentially infectious substances from the
tonsils (McKenzie, 1994).

One of the most well documented features of
yawning relates to its circadian variation. In
humans, yawning occurs with greatest frequency
within the hours just after waking and right
before sleeping (Baenninger et al., 1996;
Giganti and Zilli, 2011; Provine et al., 1987a;
Zilli et al., 2007), and this response follows a
circadian pattern in other animals as well
(Anias et al., 1984; Miller et al., 2012a;
Zannella et al., 2015). Consistent with this
evidence, it has long been suggested that yawns
are representative of boredom, drowsiness, and
fatigue (Barbizet, 1958; Bell, 1980; Suganami,
1977); yet, it is hard to reconcile these views
with observations of Olympians yawning
immediately prior to competition, musicians
yawning while waiting to perform, and
paratroopers yawning excessively leading up to
their first free-fall (Provine, 2005). Despite
the temporal association with sleep, and the
fact that yawning frequency is positively
correlated with subjective ratings of sleepiness
throughout the day (Giganti and Zilli, 2011),
the frequency of yawning is not significantly
correlated with wakeup time, sleep time, or
sleep duration (Baenninger et al., 1996; Zilli
et al., 2007). In fact, subjective ratings of
sleepiness account for less than 30 percent of
the variance in spontaneous yawning frequency
(Giganti and Zilli, 2011). Therefore, while the
yawn/sleep relationship is significant, yawns
are not simply signals of sleepiness or
fatigue.

Due to the overt respiratory component of
yawning, one commonly held belief is that yawns
function to equilibrate oxygen levels in the
blood (e.g., Askenasy, 1989). Despite the
widespread acceptance of this hypothesis among
both the layperson and medical physicians
(Provine, 2005), it was tested and subsequently
falsified 30 years ago. Provine et al. (1987b)
demonstrated that neither breathing pure oxygen
nor heightened levels of carbon dioxide
increased yawning frequency in human
participants, though each significantly
increased breathing rates. It was also
demonstrated in this report that physical
exercise sufficient to double breathing rates
had no effect on yawning. Therefore, contrary to
popular belief, yawning and breathing are
controlled by separate mechanisms (Provine et
al., 1987b).

Instead, the powerful gaping of the jaw
appears to be the most important feature of this
motor action pattern. Patients who cannot
voluntarily open their mouth due to tetraplegia,
for example, have been reported to extensively
gape their jaws during yawning (Bauer et al.,
1980; Geschwend, 1977), suggesting that the
mandibular muscular contractions are essential
for the proper function of this response. The
importance of jaw stretching is also evidenced
by the fact that people asked to clench their
teeth while yawning report feeling left in
mid-yawn, or being unable to experience the
relief of completing a yawn (Provine, 1986).
Similarly, clenched teeth yawns are perceived as
unpleasant compared to positive hedonistic
effects attributable to normal, uninhibited
yawns.

To date, comparative research supports a
role of yawning in promoting state change (e.g.,
but not limited to, sleep/wake state changes)
and cortical arousal. Provine (1986) first
proposed the state change hypothesis based on
observations that yawning was associated with
numerous behavioral transitions. The general
hypothesis was then extended to suggest that
yawning facilitates a number of behavioral
shifts such as from boredom to alertness,
changes from one activity to another, and,
importantly, between sleeping and waking
(Provine, 1996, 2005). Consistent with this
hypothesis, a large body of comparative research
aligns with the view that yawning functions to
stimulate or facilitate arousal during
environmental transitions (reviewed by
Baenninger, 1997). In support of this, yawning
occurs in anticipation of important events and
during behavioral transitions across vertebrate
taxa. Baenninger (1997) also summarizes evidence
from endocrine, neurotransmitter, and
pharmacological studies that supports the view
that yawning is an important mediator of arousal
levels. Accordingly, it has been proposed that
the adaptive function of yawning is to modify
levels of cortical arousal. A recent
reformulation of this idea proposes that yawns
activate the attentional network of the brain
(Walusinski, 2014). This notion is supported by
research on humans, chimpanzees, and laboratory
rats, showing that yawns reliably precede
increases in activity (Anias et al., 1984;
Baenninger et al., 1996; Giganti et al., 2002;
Vick and Paukner, 2010). Individual variation in
total yawn frequency per day among humans has
also been linked to activity levels (Baenninger
et al., 1996). People who are active, for
example, tend to yawn less frequently than those
who are less active. Also consistent with the
view that yawning produces an arousing effect,
yawns are common following stressful events,
threats, and increases in anxiety (e.g., Eldakar
et al., 2017; Liang et al., 2015; Miller et al.,
2010; Miller et al., 2012b). In addition,
numerous studies have revealed that yawning is
associated with hormonally-induced penile
erection (reviewed by Baenninger, 1997), a
well-defined indicator of sexual arousal.

Further evidence for an arousing effect of
yawning comes from various neurophysiological
studies. For example, yawning in humans has been
shown to produce significant changes in heart
rate and skin conductance (Greco and Baenninger,
1991; Guggisberg et al., 2007), as well as
sympathetic nerve activity (Askenasy and
Askenasy, 1996). Research has shown that arousal
responses in laboratory rats, as measured by
electrocorticogram, are accompanied by yawning
behavior following electrical, chemical, and
light stimulation of the PVN of the hypothalamus
(Kita et al., 2008; Sato-Suzuki et al., 1998,
2002; Seki et al., 2003). Furthermore, yawning
is a common response among patients undergoing
anesthesia (Kim et al., 2002), and actually
produces a transient arousal shift as measured
by electroencephalographic (EEG) bispectral
index (Kasuya et al., 2005). This result has
been interpreted as yawning representing a
mechanism to enhance arousal during the
progressive loss of consciousness caused by
induction of anesthesia. It should be noted,
however, that other studies have failed to show
yawn-associated increases in cortical arousal as
measured by EEG (see Guggisberg et al.,
2010).

One mechanism by which yawns facilitate
state change and arousal appears to be through
enhanced intracranial circulation. Generally,
yawning produces global increases in heart rate
(Corey et al., 2011; Heusner, 1946) and blood
pressure (Askenasy and Askenasy, 1996), and the
jaw stretching and deep inhalation accompanying
yawning produces profound intracranial
circulatory alterations (Provine, 2012;
Walusinski, 2014). The constriction and
relaxation of facial muscles during a yawn
increase facial blood flow, which, in turn,
increases cerebral blood flow (Zajonc, 1985).
The deep inspiration during yawning also
produces significant downward flow in
cerebrospinal fluid and an increase in blood
flow in the internal jugular vein (Schroth and
Klose, 1992). The pterygoid plexus, a network of
small veins within the lateral pterygoid muscle
activated by yawning, operates as a "peripheral
pump" that aids venous return by the pumping
action of the pterygoid muscle during yawning
(Sinnatamby, 2006). Furthermore, cadaveric
dissections suggest that the posterior wall of
the maxillary sinus flexes during yawning, which
could serve to ventilate the sinus system
(Gallup and Hack, 2011).

In an attempt to unite the existing research
linking yawning to state change, arousal, and
enhanced circulation to the skull, it has
recently been proposed that yawns function to
cool the brain by altering the rate and
temperature of the arterial blood supply (Gallup
and Gallup, 2007). While some researchers do not
accept this as a viable explanation of yawning
(Elo, 2010, 2011; Guggisberg et al., 2010, 2011;
Walusinski, 2013), the basic predictions of the
brain cooling hypothesis have been rigorously
tested, supported and replicated. For example,
evidence from both rats and humans shows that
yawns are triggered by rises in brain
temperature and produce a cooling effect to the
brain and/or skull thereafter (Eguibar et al.,
2017; Gallup and Gallup, 2010; Shoup-Knox et
al., 2010; Shoup-Knox, 2011). Experimental
research also shows that yawn frequency can be
effectively reduced through behavioral brain
cooling methods (Gallup and Gallup, 2007). The
brain cooling hypothesis is also supported by
varying lines of pharmacological and clinical
evidence, as many medical conditions and
pharmaceutical drugs alter brain/body
temperature and yawn frequency in predicted ways
(reviewed by Gallup and Eldakar, 2013; Gallup
and Gallup, 2008). Furthermore, a growing number
of studies have documented predicted changes in
yawn frequency as a function of ambient
temperature manipulation/variation, including
data from laboratory experiments and
naturalistic observations (Eldakar et al., 2015;
Gallup et al., 2009, 2010, 2011; Gallup and
Eldakar, 2011; Massen et al., 2014; Gallup,
2016).

1.2. Contagious yawning

While spontaneous yawns are triggered
physiologically and are ubiquitous
comparatively, other forms of yawning are driven
by social stimuli. Research on some non-human
primates, for example, has shown that some
yawn-like displays, known as social tension or
aggressive yawns, appear to hold a communicative
function and are used as a threat display of the
canine teeth (e.g., Deputte, 1994; Troisi et
al., 1990; Redican, 1982). However, these
"yawns" take on a different morphology and
expression compared with typical spontaneous
yawns. In some species, the signaler, rather
than closing its eyes at the peak of the "yawn",
fixes its attention on the target during the
yawning display to monitor the effect of the
yawn on the individual. These social displays
are typically documented among non-human primate
species with sexual dimorphism in body size,
canine size, and aggressive competition (Darwin,
1872), and, in fact, sex differences in yawn
frequency among primates are lost within species
with limited sexual dimorphism in canine size
(humans, Schino and Aureli, 1989; chimpanzees,
Vick and Paukner, 2010). Therefore, researchers
have questioned whether these displays can be
classified as true yawns (Gallup, 2011).

More widespread forms of social yawning
occur as a result of sensing yawns in others.
This is known as contagious yawning (CY).
Seeing, hearing (e.g. Massen et al., 2015), or
even thinking about yawning can trigger yawns in
humans, and it is suggested that attempts to
shield a yawn do not stop its contagion
(Provine, 2005). As expected, based on this
distinct mode activation, CY does not follow the
same diurnal pattern described above for
spontaneous yawns, being much less related to
sleepiness (Giganti and Zilli, 2011). Although
the motor action patterns appear
indistinguishable from one another, CY has only
been documented within a few social
species.

Given the relatively limited comparative
evidence for CY, it can be concluded that this
response is not simply a product of being social
or gregarious, but rather serves some new social
role. From an evolutionary perspective, it has
been argued that CY is a more recently evolved
behavior derived from the primitive spontaneous
form (Gallup, 2011). Further differentiation
between these two yawn-types, which is
consistent with the proposed evolutionary
framework, can be seen in terms of the
developmental trajectory of these responses. For
example, while spontaneous yawning among humans
begins early on in utero (de Vries et al., 1982)
and is very frequent among infants (Giganti et
al., 2007), CY does not emerge until early
childhood (Anderson and Meno, 2003; Helt et al.,
2010; Hoogenhout et al., 2013).

The first findings of CY in chimpanzees, but
not in monkeys, suggested a divergence of this
trait phylogenetically separating the apes from
the monkeys. However, recent studies have
provided evidence for CY in some monkey species,
whereas the picture among the apes has become
less clear (see Table 1). Even though all
studies on chimpanzees indeed do report CY,
results on bonobos are inconsistent, and the
only study on gorillas and orangutans to date
found no evidence for CY in these species.
Consequently, the picture in the primate lineage
is far from homogenous and the evolution of CY
does not seem to be homologous. Instead, the
evidence of CY in some, but not all, more
distantly related mammal species, as well as in
a bird species (see Table 1) suggests that this
trait has evolved independently within several
lineages. Nevertheless, the lack of consistent
data on CY in multiple species within particular
lineages (e.g. only a single bird species so
far) makes any phylogenetically controlled
analysis impossible, and consequently any
conclusion about its phylogenetic history is
premature. Moreover, the field most probably
suffers from a publication bias in which null
results (i.e. absence of evidence for CY in a
given species) are less likely to be published.
Therefore, a more systematic study of CY is
needed across species of different orders or
even classes. Specifically, more studies on
reptiles and amphibians are needed. Although CY
is first and foremost a social trait,
comparisons between closely related social- and
non-social species would be particularly
informative as to study both mechanistic as well
as functional hypotheses. For example, other
socially contagious behaviors (e.g.,
gaze-following) have been documented in
non-social vertebrates (e.g. red-footed
tortoise: Wilkinson et al., 2010) that do not
show CY (Wilkinson et al., 2011).

Empirical investigations into the potential
function(s) of CY are nearly absent from the
literature, but there are currently two lines of
thought. The first proposes a primarily
communicative/signaling function to this
behavior, whereby yawns serve to signal internal
states to others within the group (Guggisberg et
al., 2010; Liang et al., 2015). Given the
characteristic social nature of this response,
it perhaps makes intuitive sense to propose such
a communicative function. However, there is no
empirical support for this perspective. There is
currently no evidence that yawning, outside of
the aforementioned threat displays in non-human
primates, provides a meaningful signal to
receivers, and it is not clear what
communicative benefits there would be to yawning
(see Gallup and Clark, 2015). Moreover, yawns
are limited in their role as social signals
because they are under minimal voluntary control
(Provine, 2012). Furthermore, any potential
signal from yawning remains nonspecific since
yawns occur under a variety of contexts (i.e.,
during changes in arousal, before and after
sleep, during boredom, transitions in activity
patterns, following stress) and are often
misinterpreted in human social settings (see
Gallup, 2011). Therefore, although CY is
inherently social, experimental research is
still needed to test the predictions of
communication hypotheses.

An alternative approach to thinking about
the potential function(s) of CY is to consider
how the neurophysiological consequences of
yawning within the individual (i.e.,
intracranial circulation, cortical arousal,
brain cooling) would impact the collective, if
passed along to members of the group. That is,
instead of viewing these two yawn-types as
independent actions, it may be useful to
consider them as the same behavior produced by
different triggers. Evolution fosters
adaptations that accumulate upon existing
architecture and, thus, both behaviors should
share fundamental mechanistic pathways and may
even possess similar functional outcomes
(Gallup, 2016). Consistent with this view,
growing research shows that physiological
variables that directly alter spontaneous yawn
frequency (i.e., those that influence brain and
body temperature) have the same effects on the
spread of yawn contagion (Eldakar et al., 2017;
Gallup and Eldakar, 2011; Gallup and Gallup,
2007, 2010; Massen et al., 2014). Therefore,
when considering the neurophysiological changes
surrounding spontaneous yawning, and the
existence of CY in some gregarious species, the
spreading of this behavior across the group
could serve to heighten collective vigilance and
facilitate an adaptive response to external
stimuli under natural conditions (Gallup and
Gallup, 2007). Although this hypothesis has not
been directly tested, Miller et al. (2012b)
provide some evidence in support of this view by
demonstrating that within small groups of
budgerigars yawning becomes more contagious
following startling auditory disturbances.
Further research is certainly needed to test
these and other functional hypotheses for yawn
contagion.

2. Contagious yawning and
empathy

2.1. Conceptual problems

Despite having a relatively poor
understanding for why CY has evolved, the fact
that CY is comparatively limited and shows a
delayed developmental pattern indicates that it
may reflect some higher-level social-cognitive
capacity. Consistent with this perspective, over
the last decade and a half, a large and growing
body of research has focused on the potential
connection between yawning and empathy (e.g.,
Platek et al., 2003; Platek et al., 2005; Palagi
et al., 2009; Campbell and de Waal, 2010, 2014;
Norscia et al., 2016). Empathy is a complex
construct, representing the ability to
understand, share and be affected by the state
and/or feelings of others (Singer et al., 2004).
Thus, if sensing yawns in others can reflexively
trigger the same response, it seems that the
action of CY could be placed within a category
of empathy. The proposed link between CY and
empathy stems from a monograph on yawning that
was published nearly 40 years ago (Lehmann,
1979), and more recently by its inclusion in the
Perception-Action-Model (PAM) proposed by
Preston and de Waal (2002, see also de Waal and
Preston, 2017). Lehmann (1979) notes that
yawning is a sign of boredom (cf. Provine and
Hamernik, 1986), and considers the latter an
emotion. Subsequently, he concludes that CY thus
constitutes emotional contagion (Lehmann, 1979).
Emotional contagion in the basic sense
represents a primitive form of empathic
processing known as state matching (Preston and
de Waal, 2002), whereby the observation of an
emotional state in another elicits the same
emotion in the observer. The contagion of an
outward sign that correlates with an emotion,
however, does not per association also indicate
that the emotion is transmitted. It seems rather
unlikely that people suddenly become bored when
they see someone yawn as a result of
uninteresting stimuli, or stressed when sensing
yawns elicited by anxiety-provoking situations.
And if so, this still needs to be empirically
verified and to date no data support such an
effect. Instead, yawns that are initiated
contagiously could be due to nonconscious
mimicry or, mechanistic at an even lower-level,
resulting from 'simple' behavioral contagion
(Thorpe, 1963; Yoon and Tennie, 2010; Zentall,
2001).

Empathy is notoriously difficult to define,
and among others (e.g. Davis, 1983; Singer,
2006), Preston and de Waal (2002) emphasize its
multifaceted nature. In their seminal paper they
specifically focus on the process and include
empathy within the PAM; i.e. they superimpose
empathy on the PAM and argue that empathy thus
includes all phenomena that share the same
mechanisms. Consequently, they continue that
this should also include facilitation behaviors
like imitation or the yawn reflex. The
hierarchical structure of their proposed model
(see also the "Russian Doll Model" in de Waal,
2008, and in de Waal and Preston, 2017) thus
specifies CY as a prerequisite for empathy
(Preston and de Waal, 2002, de Waal and Preston,
2017), which has led multiple researchers to
infer that there is a direct link between CY and
empathic processing. But, one could argue that a
brain is also a necessary prerequisite for
empathy, and, as for CY, arguing that any animal
with a basal ganglion of a particular size thus
should be empathic is based on the fallacy of
the converse, or affirming the consequent.
Instead, one should also consider that there
might be more primitive systems in which CY is
included, which do not posses empathy. CY may be
a primitive root of what evolved into empathy,
or may involve a separate trend as a social
coupling mechanism. Consequently, conceptually
there is no reason to assume that the presence
or degree of CY is representative of empathic
capacities.

2.2. A critical review of empirical
evidence

Even when considering these conceptual
shortcomings, discussion of the connection
between CY and empathy is rather persistent
within the literature, as by now many studies
have produced data that seem consistent with
several derived hypotheses that predict
inter-individual differences, developmental
trajectories and certain underlying neural as
well as hormonal or neurotransmitter patterns.
Here, we critically review these hypotheses, the
data and their implications.

2.2.1. Inter-individual
differences

2.2.1.1. Questionnaire- and cognitive
measures of empathy

Perhaps the most logical prediction derived
from the proposed link between CY and empathy is
that people who are more empathic should be more
susceptible to CY. This prediction has now been
tested in several studies using questionnaire
and cognitive measures of empathy. One obvious
limitation to these studies is that all the
tests are purely correlational and thus do not
allow for causal inference. Whereas several of
such studies indeed did show a significant
relationship between an individual's
susceptibility to CY and several questionnaire-
or cognitive measures of empathy in healthy
human populations, others find no such
connection (see Table 2). As with defining
empathy, measuring it through questionnaires and
cognitive tasks also takes a multifaceted
approach. This approach is needed when dealing
with such a complex phenomenon, but it does
impair overall analyses and the reproducibility
of results, and with regard to links to CY the
picture becomes rather unclear. For example, CY
is correlated with some scales and appears to be
unrelated to others, and to date no two studies
on CY have used the same measurements of
empathy. Notably, of the 22 identified tests for
this relationship, only six (27.3%) are
significant in the predicted direction. The
emerging literature on this topic is rather
unbalanced, with the papers showing predicted
results being most often cited when discussing
this connection. This creates a problem for
progress in the field, since one could just
as well interpret the few positive results as
false positives, or type I-errors.

2.2.1.2. Links to psychological
'disorders'

There are many other approaches to examining
the connection between CY and empathy. Rather
than looking at empathic abilities on a
continuous scale, several CY researchers have
studied populations that are impaired with
regard to empathic processing. To date,
researchers have focused on individuals with
schizophrenia and Autism Spectrum Disorder
(ASD), as both conditions have been linked with
reductions in empathy (e.g., Baron-Cohen and
Wheelwright, 2004; Derntl et al., 2009).
Consistent with the proposed link between CY and
empathy, the first studies of this nature
reported a lack of CY or diminished
susceptibility to CY in ASD patients (Giganti
and Esposito Ziello, 2009; Helt et al., 2010;
Senju et al., 2007) and in people with
schizophrenia (Haker and Rössler, 2009).
These findings were taken as strong support for
utilizing CY as a behavioral measure of empathic
processing, and drew a great deal of attention
from researchers and the media. More recent
follow-up studies have revealed that at least
for ASD patients this effect is, however, mainly
due to an attention bias; i.e. individuals with
ASD typically focus less on the facial
expressions of others. In fact, when children
with ASD were specifically instructed to fixate
on the eyes of the stimuli they were just as
likely to yawn in response to CY stimuli when
compared to typically developing children (Senju
et al., 2009). Similarly, in a study in which an
eye-tracker controlled the onset of the yawn and
control stimuli to ensure that the participants
paid attention, CY was found at similar rates
both in ASD and typically developing children
(Usui et al., 2013). Therefore, while initially
this line of research was quite promising and
widely cited in support of the CY/empathy
connection, further research in this area has
cast doubt on this interpretation.

2.2.1.3. Sex differences

The potential for sex differences in CY has
also recently been explored. Quite some research
by now has revealed that there is a strong
difference in empathic qualities between men and
women (reviewed in Christov-Moore et al., 2014),
and thus Norscia et al. (2016) predicted that
the susceptibility of CY, as a proxy for
empathy, should be lower among men in comparison
to women. When these authors then indeed found a
difference between men and women in CY using
observational methods, they used this as
evidence to back up the claim that CY is indeed
a marker of empathic processing. Aside from
representing circular reasoning, the authors did
not find a difference in CY susceptibility
between men and women. What they report is a
difference in the frequency of yawns, following
exposure to yawns from others, between men and
women that were already shown to be susceptible,
thereby greatly reducing their sample. This
remains the only reported sex difference in CY
among humans despite numerous psychological
investigations of this behavior in men and
women, and in a review of the existing
literature, we (Gallup and Massen, 2016) found
no support for such a bias. Of the 17 other
previously published studies that analyzed for
sex differences, and the one since then (Eldakar
et al., 2017), no such difference was found. The
lack of a sex difference in CY appears to be a
robust and highly reproducible effect. The sole
sex difference presented by Norscia et al.
(2016) thus seems a false positive. Moreover,
this effect has not been demonstrated in any
other animal species (see Table 1), though it is
unclear whether other non-human animals show sex
differences in empathy.

Within the comparative literature, several
studies show sex differences in CY, but these
depend on the sex of the initial yawner rather
than the observer (see Table 1). These patterns
are opposite for the two pan species; i.e. among
chimpanzees the yawns of males are more
contagious (Massen et al., 2012), whereas among
bonobos the yawns of females are more contagious
(Demuru and Palagi, 2012). This pattern may
reflect attention biases towards the more
dominant group members (cf. Emory, 1976; Deaner
et al., 2005) and a subsequent higher likelihood
of CY, because in chimpanzee societies males are
the dominant sex whereas among bonobos females
are of higher rank. Two studies reported an
interaction effect of the sex of the stimulus
and of the responder. Massen et al. (2012) found
that CY in chimpanzees was especially prevalent
among male responders, while Palagi et al.
(2009) found that CY in gelada baboons is much
more common among females. Again, rather than
supporting a connection with empathy, this
differential response could be explained by
attentional biases due to the dominance
structure of chimpanzee societies and the
matrilineal structure of gelada societies.

By far, the majority of studies examining
the proposed link between empathy and CY have
tested for familiarity/in-group biases in this
response. The idea being that empathy increases
with the degree of familiarity between
individuals (reviewed in Preston and de Waal,
2002), and if CY is indeed a proxy for empathy,
the probability of yawn contagion should also
increase with familiarity of the stimulus (first
spontaneous yawner) to the responder. Indeed,
several studies in humans (Norscia and Palagi,
2011; Palagi et al., 2014; Norscia et al., 2016;
but see Massen et al., 2015), and in other
animals (see Table 1) show that CY
susceptibility is higher when the stimulus is of
the same group, a kin member, or a friend, and
correlates positively with measures of
relationship quality or social closeness.
However, the evidence for a familiarity bias for
CY is quite mixed comparatively, with several
other studies failing to find such a
relationship (see Table 1).

Although consistent with an underlying
connection with empathy, a higher incidence of
CY between familiar individuals suffers from a
large confound related to the issues already
mentioned, namely that attention in general is
biased by familiarity: humans (Méary et
al., 2014) but also monkeys (Whitehouse et al.,
2016) for example show an attention bias towards
in-group members, or kin (Schino and Sciarretta,
2016), and away from unfamiliar conspecifics. In
fact, in humans gaze avoidance is common among
strangers in both natural and experimental
contexts (Zuckerman et al., 1983; Laidlaw et
al., 2011). Moreover, research shows that humans
detect the faces of in-group members quicker
(Jackson and Raymond, 2006), and facial identity
and expression are perceived more integrally
when the face is more familiar (Ganel and
Goshen-Gottstein, 2004). Additionally, in-group
faces are perceived more holistically than
out-group faces (Michel et al., 2006), and
familiarity increases the detection of visual
change in faces (Buttle and Raymond, 2003), like
for example when someone starts yawning.

Importantly, several studies examining the
relationship between CY and familiarity have not
considered attention biases at all. Some
researchers controlled for attention biases by
excluding individuals from their analyses that
did not pay attention (Palagi et al., 2009;
Massen et al., 2012; Romero et al., 2014), by
only showing stimuli when subjects were paying
attention (Romero et al., 2013), or by repeating
a stimulus when an individual was not paying
attention (Madsen et al., 2012, 2013). Others
measured the effect of attention and found
either no difference in general attention
between familiar or unfamiliar (Silva et al.,
2012), in-group out-group (Gallup et al., 2015),
and even differences in the direction opposite
to the prediction (i.e. out-group > in-group:
Campbell and de Waal 2011, 2014).

However, attention is difficult to define
(when is someone paying attention?), and general
attention may not be so informative given the
specific biases mentioned above. Two studies so
far, have used an eyehole while experimentally
showing chimpanzees yawn stimuli, which should
guarantee attention, and still find an in-group
bias (Campbell and de Waal, 2011), and a
familiarity bias in inter-species contagion with
regard to chimpanzees catching yawns from either
familiar or unfamiliar humans (Campbell and de
Waal, 2014). Whereas we applaud this method to
account for biases in general attention, it
remains unclear exactly what the chimpanzees in
these experiments, or the animals/humans in any
other study are paying attention to; e.g. the
actual yawn of the individual in the stimulus,
or more specific features, like in the example
of out-group chimpanzees, the size of its
canines (see above)?

In sum, a familiarity bias for CY is far
from universal across species tested so far
(Table 1), and unless researchers can rule out
the confound of familiarity biases in general
attention and implement measures for monitoring
what individuals are paying attention to in CY
studies, any documented familiarity bias in CY
remains inconclusive with regard to the proposed
link between empathy and CY. Furthermore, it is
important to highlight that an in-group or
familiarity bias in behavioral contagion can be
explained without any connection to empathy.
Behavioral coupling of a neurophysiological
response like yawning could be adaptive in a
variety of ways (i.e., group coordination and
vigilance, Miller et al., 2012b; Gallup et al.,
2017), and it is even possible that CY is a
non-adaptive byproduct of social facilitation
that evolved in the context of ecologically
relevant group coordination.

2.2.2. Developmental

Whereas spontaneous yawning has been
recorded in fetuses of 11 weeks and older (de
Vries et al., 1982; Reissland et al., 2012), its
contagious counterpart normally does not emerge
before the age of 4&endash;5 years (Anderson and
Meno, 2003; Millen and Anderson, 2010; Helt et
al., 2010). Similar ontogenetic patterns have
been reported for chimpanzees, geladas and dogs,
whereby CY among juveniles is lower when
compared to adults (Madsen and Persson, 2012;
Madsen et al., 2013; Palagi et al., 2009).
Additionally, the contagiousness of yawning
seems to wane in old age (Giganti et al., 2012;
Massen et al., 2014; Bartholomew and Cirulli,
2014), though this result needs to be taken with
caution as it may be due to a general decrease
in yawn frequency among the elderly (Zilli et
al., 2008) and/or visual and auditory sensory
decline. The relatively late development and
subsequent decrease in CY among elderly
populations is consistent with the developmental
stages of empathy, of which some also only
develop relatively late (see below) and diminish
at old age (Maylor et al., 2002). However, the
fact that the developmental trajectories, or the
first occurrence, of specific traits are in
parallel does not mean they are directly linked,
and could be due to other factors. Moreover, the
age at which CY emerges in children occurs when
cognitive facets of empathy are also developing
rather than the more 'simple' responses like
emotional contagion (newborns: Hoffman, 1982;
Singer, 2006), or the development of
self-awareness, as measured by the mirror-mark
test (age 18&endash;24 months; Amsterdam et al.,
1972). In fact, the development of CY parallels
that of first order mentalizing, or theory of
mind, as attested by the Sally&endash;Ann test
(Baron-Cohen et al., 1985; Perner et al., 1987).
Nevertheless, there have been no explicit
connections between CY and theory of mind,
probably since the latter has been notoriously
difficult to evaluate in animals that
nonetheless show CY, or for that manner in
non-human animals in general (but see Krupenye
et al., 2016).

Moreover, similar to the differences between
ASD and typically developing individuals, some
of the sex differences between animals, and
possibly the familiarity effects described
above, at least one study investigating CY in
children indicates that the developmental
effects are due to a lack of attention to the
stimulus presentation. When, for example,
children at the age of 3 years where primed to
make eye contact before witnessing a yawn, they
also displayed CY (Hoogenhout et al., 2013).
Similar developmental patterns regarding
attention in non-human animals (e.g.
chimpanzees: Bard and Leavens, 2014; dogs:
Wallis et al., 2014) may, consequently, also
account for the developmental patterns of CY in
these species. And finally, the inverted
U-shaped developmental trajectory of attention
in humans (Craik and Bialystok, 2006), with a
decrease with senescence (e.g. Quigley et al.,
2010), may also explain the reduction of CY in
the elderly. Future research is needed to
examine this possibility.

2.2.3. Brain studies

The proposed link between CY and empathy has
also garnered a lot of interest within studies
employing neuroimaging methods, whereby
researchers can examine how humans exposed to
yawn stimuli show increased activity in areas of
the brain implicated in empathic processing,
such as the mirror neuron system (e.g., Cooper
et al., 2012; Haker et al., 2013). The argument
here is that to empathize or sympathize with
someone, we need to be able to project that
individual's feelings or emotions onto our own
mind first, before we can act appropriately
(Leslie et al., 2004). Mirror-neurons that fire
both when observing an action and when
performing that action (di Pellegrino et al.,
1992) seem to be able to fulfill that function.
Note, however, that mirror neurons are de facto
motor neurons, and whereas they are able to
mirror movement and/or emotional expressions
(Leslie et al., 2004), they are from a
conceptual point of view not necessarily
involved in the (brain's) interpretation of
these actions. Consequently, assuming a causal
link between the two should be avoided (Lamm and
Majdand_i_, 2015).

To date, the results with regard to the
involvement of mirror neurons in CY are
inconsistent, as a number of studies fail to
show any increase in activity within these brain
regions while observing yawning stimuli
(Schürmann et al., 2005; Platek et al.,
2005). These and other studies, however, show
specific activation in a variety of other brain
areas that have been linked to empathy-related
capacities; i.e. the right posterior superior
temporal sulcus and bilaterally in the anterior
STS (Schürmann et al., 2005), the posterior
cingulate and precuneus (Platek et al., 2005),
the ventromedial prefrontal cortex (Nahab et
al., 2009), and the right posterior inferior
frontal gyrus (Arnott et al., 2009). In fact,
the most consistent feature of neuroimaging
studies examining CY is their inconsistency.
Whereas one could argue that the increased
activity of multiple areas across these samples
reflects the multi-faceted connection between CY
and empathy, they are not activated in parallel
across different studies, and the single
neurological components linked with empathy may
perform different functions when activated alone
compared to when the system operates as a whole
(Bechtel 2008). As a larger issue with
functional imaging studies, the activation of
one single brain area may result in multiple
behavioral patterns (Krakauer et al., 2017), and
consequently it is difficult to draw causal
relationships. Therefore, behavioral studies are
still needed (Krakauer et al., 2017), and
behavior is exactly what is missing in these
neuroimaging studies.

Specifically, while these studies claim that
they show the activation of particular brain
regions involved in CY, what they actually show
is how the brain reacts to sensing yawns in
others, and the contagiousness of this response
is either suppressed, as participants are not
allowed to move in imaging studies, not reported
in for example the one EEG study (Cooper et al.,
2012), and possibly absent. In one study
participants had to score whether they felt
contagion or not (Haker et al., 2013), yet the
analyses were not restricted to those
contagiously rated stimuli. In another study the
participants were asked to rate the
contagiousness of auditory stimuli on a 4-point
scale (Arnott et al., 2009), and here they
indeed showed that activity of the right
posterior inferior frontal gyrus was highest
after listening to yawn stimuli that were rated
highly for contagion. However, the stifling of
CY responses either through collars or
constraining cushions (Nahab et al., 2009;
Schürmann et al., 2005), or because
participants were told to lie still (Arnott et
al., 2009; Haker et al., 2013), deserves careful
consideration, since in and of itself this could
involve heightened self-awareness (cf. Provine,
1986) and subsequent activation of empathy
related brain areas specifically during exposure
to yawn stimuli.

Another important and related issue to
consider is how the widespread social stigma
surrounding yawns may impact these studies.
Because yawning is often considered rude or
disrespectful (Schiller, 2002), and CY appears
to be actively inhibited by social presence in
laboratory settings (Gallup et al., 2016b),
simply sensing yawns during an imaging
experiment could activate areas more generally
related to social cognition (Takahashi et al.,
2004). Thus, neuroimaging studies reporting
areas of brain activation in response to yawning
stimuli should be interpreted with caution.

One study recently investigated whether the
administration of intranasal oxytocin alters CY
in a sample of male college students (Gallup and
Church, 2015). Given that oxytocin has been
implicated in various forms of empathic
processing (Gonzalez-Liencres et al., 2013; De
Drue and Kret, 2015), and intranasal oxytocin
increases emotional empathy in men (Hurlemann et
al., 2010), one might expect that it should also
increase the susceptibility of yawn contagion.
However, while the results clearly demonstrated
a change in behavior from that intranasal
oxytocin, this manipulation did not increase CY
susceptibility. In fact, oxytocin appeared to
inhibit the expression of yawning, perhaps by
enhancing social awareness of this response (see
above). These findings and others highlight the
complex social nature of CY in humans.

3. Future directions

Despite the rather inconsistent and indirect
empirical evidence reviewed above, we are not
advocating that researchers should discard the
possibility of a direct connection between
empathy and CY. Particularly, the ability to
identify a behavioral marker of empathy, a
phenomenon that has been notoriously difficult
to define (or measure for that matter), would be
of tremendous impact to the behavioral sciences.
Unfortunately, direct tests for a connection
between CY and empathy are lacking. Therefore,
we propose some methodological and conceptual
advances that could be made to more explicitly
test this connection. In addition, we briefly
highlight some more general methodological
issues within the study of CY.

We propose that future research examining
the link between CY and empathy begin to focus
on the use of experimental methods, while
including a more multifaceted approach to
measuring empathy (e.g., cognitive vs.
emotional, multiple subjective and objective
measures). In particular, a fruitful yet
previously overlooked approach to studying this
connection would be to directly manipulate one
variable to witness its effects on the other. If
CY represents a primitive form of empathy, then
manipulating empathic responses should alter the
expression of CY. To date, only one study has
attempted to employ such an approach through the
peripheral administration of oxytocin in humans
(Gallup and Church, 2015). Similarly, if CY
activates neural pathways tied with empathic
processing, studies could actively induce or
inhibit CY to test how this alters empathy
responses thereafter. This research approach
could investigate how a combination of both
subjective and objective (neurophysiological)
measurements of varied forms of empathy (1)
correlate with, (2) affect, and (3) are affected
by CY. Future research in this area, both on
humans and non-human animals, should help
elucidate the proposed empathy/CY
connection.

Moreover, we argue that the study of CY
would be improved by a greater recognition that
spontaneous and contagious forms of yawning
represent the same behavior produced by
different triggers. These yawn-types are
indistinguishable in their motor action
patterns, and thus should produce similar
neurophysiological effects thereafter. We feel
that future research should approach CY from the
bottom up as a behavioral phenomenon first, and
then investigate it with a holistic approach
taking into account all 4 of Tinbergen's
considerations (Tinbergen, 1963). Consequently,
researchers should not only consider
developmental and/mechanistic questions about
CY, but as mentioned before, also focus more on
potential functional explanations of CY (e.g.,
group vigilance; Gallup and Gallup, 2007; Miller
et al., 2012b) and more rigorously investigate
its phylogeny to elucidate whether CY has
emerged through convergent, parallel or
homologous evolution.

3.1. Methodological problems and
advances

In 2010, Campbell and de Waal wrote a very
informative paper on the methodological problems
in the study of CY (Campbell and de Waal, 2010).
They argued, rightfully, that the field suffers
from a strong variation in methods used to study
CY, which makes comparisons between studies very
difficult. Fortunately, some of their issues are
partly resolved and by now, for example, most
experimental studies do use a non-yawn stimulus
as a control condition to compare yawning rates.
Additionally, Campbell and de Waal (2010)
noticed that there are large between-study
differences in the number of yawns displayed to
subjects and the duration of the yawns shown.
Whereas recent studies show that the latter
represents biologically relevant variation
(Gallup et al., 2016a), the former remains a
problem when comparing results between studies.
Though it should be noted that for proof of
concept tests (CY in a species; yes or no?),
when well controlled, this does not constitute a
problem. Campbell and de Waal (2010), also
noticed differences with regard to the analyses
used within various studies; i.e. either
population level comparisons of yawn frequencies
in yawn and control conditions, or binomial
analyses of whether an individual yawned or not
in either condition. Studies using the latter
method often report percentages of individuals
that showed CY and Campbell and de Waal (2010)
argued that these percentages are not
informative given the wide range of stimuli
used. However, the comparisons of yawn
frequencies between test and control conditions
can suffer from the self-contagious effect of
yawning (i.e., one yawn often triggers several
subsequent yawns in the same individual a.k.a.
yawn bursts; e.g. Giganti and Salzarulo, 2010),
so we advocate for the use of both analyses.
Most importantly, however, we agree with
Campbell and de Waal (2010) that authors must
acknowledge the differences in methods used when
making comparisons between existing
studies.

Whereas we encourage the use of experimental
tests of CY as it allows for an easier
determination of different variables that may or
may not influence this response, we acknowledge
that observational studies of CY are paramount
for our understanding of its ecological
relevance (e.g. function). The problem with
observational studies, however, is the
difficulty in defining whether a yawn is
spontaneous versus when it is caused by sensing
another yawn. This difficulty becomes apparent
in the literature particularly when comparing
the timeframes within which a second yawn is
considered dependent on/infected by the previous
(see Kapitány and Nielsen, 2017): e.g. 20
s. (Miller et al., 2012b) vs. 5 min. (Palagi et
al., 2009). Whereas first of all it seems rather
implausible that the contagious effect of a yawn
can last 5 min, increasing these timeframes in
the absence of comparable control conditions
also significantly increases the possibility
that some spontaneous yawns are considered
contagious (Kapitány and Nielsen, 2017).
Generally, studying CY observationally by
defining a yawn to be caused by another yawn of
a different individual within a certain time
ignores the (random) distribution of spontaneous
yawns and thus may contain false positives. This
problem becomes less problematic when using very
short timeframes, but the measurement of CY is
nevertheless influenced by an
individual's/species' frequency of spontaneous
yawning, which in turn may be influenced by
several factors (see introduction). Therefore,
we advise testing whether the observed
'clumping' of yawns and the frequency of such
'clumps' differs from random behavior; i.e.
random 'clumps' of spontaneous yawns (cf. Sokal
and Rohlf, 1995), as has been done in some
non-human studies (budgerigars: Miller et al.,
2012a,b; marmosets: Massen et al., 2016).
Additionally, a comparison of presumed CY with
baseline rates of spontaneous yawns using
survival analysis may be a useful approach
(Schino et al., 2009).

Finally, we highlight recent technological
advances that could allow for better and more
controlled studies of CY in relation to empathy.
First, as attested by our review of the
literature above, attention biases remain a
large confound within this literature. Recent
advances in eye-tracking have given us a very
powerful tool to examine what people are paying
attention to, and this method has now also been
reliably used to study attention biases in
non-human animals including apes (Krupenye et
al., 2016) and dogs (Somppi et al., 2013).
Therefore, when studying inter-individual
differences in CY, the use of eye-tracking
devices can help determine in more detail what
humans and other animals are attending to within
the stimulus presentation. Eye-tracking data
could also be used for assuring equal exposure
to test or control stimuli, familiar or
unfamiliar stimuli, or of individuals from
different populations (cf. Usui et al.,
2013).

Second, with regard to brain imaging
research we highlighted the problem that
subjects within these studies are forced to
inhibit their yawn responses, and that such
inhibition in a laboratory setting may introduce
a confound regarding neurological activity
measured in the brain. Unfortunately, real-time
fMRI remains very vulnerable to movement
artifacts (Magland and Childress, 2014).
Therefore, we welcome neuroimaging studies that
allow subjects to actually yawn when they feel
the urge to do so, using methods that are robust
to such movement. For example, recent advances
in EEG hardware and analyses now allow this
method to be used when subjects are in motion,
opening novel research opportunities (Reis et
al., 2014). Similarly, albeit with lower
definition, near-infrared spectroscopy and
topography (Jobsis, 1977) allows for movement,
and has, for example, recently been suggested as
a useful tool to characterize children with ASD
(Li et al., 2016). Such technological advances,
when applied appropriately to the study of CY,
would greatly improve our neurobiological
understanding of this phenomenon and could help
elucidate possible links between CY and
empathy.

4. Conclusion

In this review, we critically evaluated the
research on the proposed link between CY and
empathy. We first question the conceptual basis
for this link, and second find the current
empirical evidence supporting this connection to
be indirect, inconclusive and in some cases
absent. The aforementioned review of the
literature demonstrates results that are mixed
and inconsistent with regard to this
association. For nearly all areas examined,
there exist studies reporting data both for and
against the proposed association. Studies
examining inter-individual differences related
to empathy and CY provide evidence that is quite
contradictory, and in fact, differences in
empathy measures in humans prove to be a poor
predictor of CY (see Table 2). Despite the fact
that women have repeatedly been shown to score
higher on empathy measures, only one study has
reported any difference in the expression of CY
between men and women, though the susceptibility
to CY remained the same. Experiments examining
CY within populations with well-defined deficits
in empathy, such as ASD, provide mixed support
for this connection depending upon whether
participants are instructed to pay attention to
the stimuli presented within the study.
Furthermore, the large and growing body of
studies investigating in-group/familiarity
biases in CY provides no overall trend,
particularly within the comparative literature.
The majority of these studies also suffer from
confounds related to biases in the degree and
types of visual attention toward in-group versus
out-group members, or related to levels of
affiliation. The overlap in the developmental
trajectory of CY and empathy is certainly
consistent with a connection between the two,
but this remains correlational and further
research is needed to more closely examine the
development of empathic processing and the
susceptibility to CY in tandem. Recent data also
shows that ontogenetic changes in CY may be more
related to changes in visual processing. The
various neuroimaging studies show no clearly
convergent or consistent areas of activation
within the brain following exposure to yawn
stimuli, and fail to consider confounds related
to the active inhibition of this response and
social stigma of yawning when in the presence of
others. When taken together, the proposed
connection between CY and empathy should be
viewed with caution. We propose the use of more
rigorous and direct experimental manipulations
to explicitly test this connection within future
research.

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